Ann. Limnol. - Int. J. Lim. 52 (2016) 379–386 Available online at: Ó The authors, 2016 www.limnology-journal.org DOI: 10.1051/limn/2016022

Aplexa hypnorum (Gastropoda: Physidae) exerts competition on two lymnaeid species in periodically dried ditches

Daniel Rondelaud, Philippe Vignoles and Gilles Dreyfuss* Laboratory of Parasitology, Faculty of Pharmacy, 87025 Limoges Cedex, France

Received 26 November 2014; Accepted 2 September 2016

Abstract – Samples of adult Aplexa hypnorum were experimentally introduced into periodically dried ditches colonized by Galba truncatula or Omphiscola glabra to monitor the distribution and density of these snail species from 2002 to 2008, and to compare these values with those noted in control sites only frequented by either lymnaeid. The introduction of A. hypnorum into each ditch was followed by the progressive coloni- zation of the entire habitat by the physid and progressive reduction of the portion occupied by the lymnaeid towards the upstream extremity of the ditch. Moreover, the size of the lymnaeid population decreased significantly over the 7-year period, with values noted in 2008 that were significantly lower than those recorded in 2002. In contrast, the mean densities were relatively stable in the sites only occupied by G. truncatula or O. glabra. Laboratory investigations were also carried out by placing juvenile, intermediate or adult physids in aquaria in the presence of juvenile, intermediate or adult G. truncatula (or O. glabra) for 30 days. The life stage of A. hypnorum had a significant influence on the survival of each lymnaeid. In snail combinations, this survival was significantly lower for adult G. truncatula (or O. glabra) than for intermediate snails. In contrast, the survival of juveniles was similar to that noted in the corresponding controls. This interspecific competition between the physid and either lymnaeid may not be due to food present in their habitat, but might be due to the toxicity of mucus secreted by intermediate and adult A. hypnorum.

Key words: Aplexa hypnorum / colonization / density / ditch / Galba truncatula / Gastropoda / Lymnaeidae / Omphiscola glabra / Physidae

Introduction populations because of the summer drought which was too short: 5–6 weeks (Rondelaud et al., 2006). A terrestrial Fasciolosis due to Fasciola hepatica (Linnaeus) has a snail, Zonitoides nitidus (O.F. Mu¨ ller), able to actively worldwide distribution, with human and animal cases prey on these lymnaeids, was also applied in several cattle- being reported on the five continents. To accomplish its breeding farms. However, this method has not become life-cycle, this fluke needs a definitive host (generally a generalized because of the complexity of applying this mammal) that harbours the adult parasite and an inter- control in the field by non-specialists (Rondelaud et al., mediate host (a freshwater pulmonate gastropod) that 2006). ensures the development of larvae. In Western Europe, the Another method of control is to use a freshwater snail, most common host snail is Galba truncatula (O.F. Mu¨ ller) which is not a compatible host for F. hepatica,asa (Taylor, 1965; Torgerson and Claxton, 1999). Another competitor of these lymnaeid populations. Several gastro- lymnaeid, Omphiscola glabra (O.F. Mu¨ ller) also can sus- pods have already been used as competitors in the past tain larval development of F. hepatica (Abrous et al., 1999, to control intermediate hosts for schistosomes, but the 2000; Rondelaud et al., 2015). The control of these success of these biological agents varied according to the invertebrate populations has been proposed by numerous snail species and the country in which they were intro- authors as one of the means to eliminate the fluke from duced (Brown, 1994). As no freshwater pulmonate gastro- farms (Taylor, 1965). On the acidic soils of central France, pod was reported as a competitor of G. truncatula and the use of open drainage only limited the size of snail O. glabra in the literature, it was reasonable to search for a candidate among species belonging to the same *Corresponding author: [email protected] snail community. In Western Europe, these lymnaeids are Article published by EDP Sciences This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited 380 D. Rondelaud et al.: Ann. Limnol. - Int. J. Lim. 52 (2016) 379–386 known to live in periodically dried habitats with the physid Aplexa hypnorum (Linnaeus) and planorbids such as Anisus leucostoma (Miller) or A. spirorbis (Linnaeus) (Costil et al., 2001; Vignoles et al., 2015). As another physid, Physella acuta (Draparnaud) was already reported as a competitor against Bulinus truncatus (Audouin) in Egypt (El-Hassan, 1974), the competition of A. hypnorum against G. truncatula and O. glabra was investigated. A. hypnorum is known for its distribution in most European countries (Welter-Schultes, 2012, 2013) and North America (Dillon et al., 2006). But in some countries, the numbers of these snails were small such as in woodland ponds from Southern Poland (Spyra, 2010) and a few ponds of the upper Rhine valley (Mosimann, 2000; Bauer and Ringeis, 2002). This physid colonizes small and temporary waterbodies rich in veg- etation, located in lowlands. It is also found on swampy and forested margins of lakes, in swampy deciduous forests, and very moist meadows (Welter-Schultes, 2013). However, the species prefers ditches, temporary ponds Fig. 1. Location of the ten road ditches in the Brenne Regional and pools, which it shares with other gastropod species Natural Park, department of Indre (Central France). adapted to seasonal habitats (Kerney, 1999; Anderson, 2006). The bottom of these habitats often consisted of Materials and methods mud (Glo¨ er and Diercking, 2010). In addition, a positive relationship was noted in Germany between the abun- Snail identification was done on the basis of shell shape dance of snails and sand and/or clay soil types (Den and size, and also length of reproductive organs according Hartog, 1963; Glo¨ er and Diercking, 2010). The future of to the keys by Glo¨ er and Meier-Brook (2003). A. hypnorum is particularly worrying in Western European countries due to destruction of its moist habitats owing to land drainage and the general intensification of agriculture Field investigations (Kerney, 1999). In these periodically dried habitats, community dy- Snail habitats namics depend on species-specific abilities to withstand drought periods (Dillon, 2004). However, periodic The field part of the investigation included a total of drought is not the sole factor that acts on the dynamics ten ditches inhabited by either G. truncatula or O. glabra. of these populations, as the composition of this freshwater These ditches were located within the municipalities pulmonate community also has also an effect on variations of Chitray, Luzeret, Migne´ and Thenay, department of in snail numbers. In the Brenne Regional Natural Park Indre, Central France (Fig. 1). The first six ditches (Central France), the densities of adult O. glabra were were only inhabited by G. truncatula in March 2002. At similar when this lymnaeid was living alone or with this date, 50 adults (shell height >12 mm) of A. hypnorum A. spirorbis in its habitat. In contrast, the size of each from a nearby upstream pond (46x45k14kkN, 1x11k7kkE) O. glabra population fell strongly when A. hypnorum or were introduced in the deepest zone of each of three P. acuta occupied the same habitats (Vignoles et al., 2015). G. truncatula ditches (46x35k53kkN, 1x27k27kkE; 46x36k38kkN, In view of these results, the two following questions 1x27k10kkE; 46x40k33kkN, 1x22k44kkE). The remaining arose: was competition for trophic resources between three G. truncatula-only ditches (46x35k2kkN, 1x27k18kkE; A. hypnorum and O. glabra the reason for the observed 46x36k40kkN, 1x27k8kkE; 46x40k27kkN, 1x21k23kkE) served as population dynamics in coexistence? Might the numerical controls. The length and area of these first six habitats decrease of O. glabra result from a lethal action of ranged from 42 to 87 m and from 18.9 to 39.1 m2, respec- A. hypnorum on eggs and juveniles of the lymnaeid? tively, in March 2002. Following the same methods To answer the first question, field investigations were as above, 50 adult A. hypnorum were introduced to carried out during seven successive years to monitor the the deepest zone of each of two O. glabra-only ditches dynamics of G. truncatula and O. glabra populations living (46x33k37kkN, 1x24k18kkE; 46x40k17kkN, 1x18x3kkE), while in ditches where A. hypnorum was experimentally intro- the other two O. glabra ditches (46x34k47kkN, 1x24k34kkE; duced. The answer to the second question was provided 46x42k47kkN, 1x19k69kkE) served as controls. The length by monitoring population dynamics in laboratory aquaria of these last four habitats ranged from 81 to 146 m in with A. hypnorum and G. truncatula or O. glabra. In March 2002 and their area from 36.4 to 65.7 m2. The both cases, controls were road ditches colonized by longest distance between these ten snail habitats was G. truncatula or O. glabra (but without A. hypnorum), or 18 km. All these ditches contained rain water during most aquaria containing G. truncatula or O. glabra only. of the year (from the end of October to mid-June). D. Rondelaud et al.: Ann. Limnol. - Int. J. Lim. 52 (2016) 379–386 381

The bottom sediment was composed of silt and sand, Kruskal–Wallis test was used to compare snail densities and was supported by impermeable subsoil generally noted in each quadrant in 2002 and 2008. All the statistical formed by sandstone and/or clay. Water pH varied from analyses were performed using Statview 5.0 software (SAS 6.7 to 7.8 and the dissolved calcium level ranged from 26 Institute Inc., Cary, NC, USA). to 35 mg.Lx1 (Dreyfuss et al., 2010). In the G. truncatula habitats, vegetation was mainly composed of scattered clumps of rushes. Numerous rush clumps and a few pond- Laboratory investigations weeds grew in the O. glabra habitats. In all these ditches, there were detritus during most of the year and epiphytic The behaviour of G. truncatula or O. glabra in the filamentous algae in spring. These habitats were subjected presence or the absence of A. hypnorum was studied during to the same climatic conditions, with a wet temperate three successive years between 2010 and 2013. Three life climate modulated by westerly oceanic winds. The stages were considered for A. hypnorum and O. glabra: mean annual precipitation noted during the 50 years pre- juveniles (2–3 mm), intermediates (4–5 mm) and adults ceding field investigations is 800 mm, while the mean (12–13 mm). In the case of G. truncatula, shell heights annual temperature is 10.5–11 xC(Dreyfuss et al., 2010; of the three life stages were 1.5–2, 3–4 and 6–7 mm, Rondelaud et al., 2011). Mean annual values recorded respectively. The A. hypnorum were collected in March for each parameter during the years of investigation were from a small pond (46x45k14kkN, 1x11k7kkE), while the similar to those reported above. G. truncatula originated from a road ditch (46x40k24kkN, 1x20k45kkE) and the O. glabra from another road ditch Protocol of investigations (46x41k0kkN, 1x25k33kkE) located in the municipalities of Nuret-le-Ferron and Chitray, respectively. All snails During seven successive years (2002–2008), snails were collected from the field were subjected to a 48-h period counted in mid-May in the ten ditches during the warmest of acclimatization to laboratory conditions (see below) hours of the day (1–4 p.m.) because they were present at before being used for experiments. As parasitism may have that time in the upper layer of water. This period was an effect on snail ecophysiology, reproduction output and chosen because all snails belonging to the spring and/or behaviour (Zbikowska, 2011), 50 snails for each species overwintering generations were at the adult stage. First, and each life stage were collected each year from their the length of the ditch colonized by each species was deter- natural habitat in March and were dissected in the lab- mined by noting the presence or absence of the snail from oratory under a stereomicroscope to detect the presence of the downstream to the upstream parts of each habitat. monogenean or digenean larval forms. Secondly, eight quadrants of 1 m2 each (A–H), located Each life stage of A. hypnorum was introduced into a from the downstream to the upstream parts of each covered 5-L aquarium containing lymnaeids (G. truncatula habitat and separated from each other by a 3–6 m interval or O. glabra) which had the same or a different life stage. (habitats with G. truncatula) or 6–12 m interval (those with The number of snails per recipient was five physids and ten O. glabra), were selected in each ditch to count snails. In lymnaeids. These snail numbers were selected on the basis each quadrant, snails were collected using a 20-cm dia- of snail densities noted in May 2008 in ditches colonized meter sieve (mesh size, 3 mm) if the depth of the water by A. hypnorum (see above). Tables 1 and 2 indicate the layer was more than 10 cm or by sight in the other cases different types of pairwise combinations formed with the (water depth less than 10 cm, or reduced to a film). This physid and either lymnaeid (nine types of combinations in area was controlled 15 min later to collect snails that could each case). Five aquaria were used each year for each snail have escaped during the first count. Snails were then combination (a total of 25 individuals for A. hypnorum and classified according to their species before being replaced 50 for either lymnaeid). Following the same method, in each area. control groups were constituted for each snail species and each life stage. Three replicates for each snail combination Parameters studied or each control group were performed in March between 2010 and 2013. All aquaria were placed at a constant The first parameter considered was the length of temperature of 20x¡1 xC and a natural photoperiod the ditch colonized by each snail species over the 7-year of 12 h light. The dissolved calcium content in spring period. Values recorded at the sites occupied by water was 35 mg.Lx1. Pesticide-free, dried lettuce leaves A. hypnorum and G. truncatula or by G. truncatula only and dead Molinia caerulea leaves were given ad libitum as were pooled and expressed as percentages in relation to food for snails. Each week, spring water and food were the total length of each habitat (Fig. 1(A) and (B)). A changed. After 1 month, physids and/or lymnaeids similar protocol was also used for values noted in habitats surviving in each aquarium were counted. colonized by A. hypnorum and O. glabra or by O. glabra The parameter for the three snail species was the only (Fig. 1(C) and (D)). The second variable was the number of live individuals on day 30 of the experiment. density of each snail species in the eight 1-m2 quadrants of Normality of snail numbers was analysed using the each habitat. Normality of snail densities was analysed Shapiro–Wilk test (Shapiro and Wilk, 1965). As the dis- using the Shapiro–Wilk test (Shapiro and Wilk, 1965). As tribution of these values for G. truncatula was not normal, the distribution of these values was not normal, the the Scheirer–Ray–Hare test coupled with the Steel-Dwass 382 D. Rondelaud et al.: Ann. Limnol. - Int. J. Lim. 52 (2016) 379–386

Fig. 2. Length (%) of habitat colonized by each snail species over a 7-year period: A. hypnorum and Galba truncatula (2A), A. hypnorum and Omphiscola glabra (2B), G. truncatula only (2C) and O. glabra only (2D). post-hoc test (Siegel and Castellan, 1988) was used to significantly lower than in 2002 (Fig. 3(B)). In control compare the differences between the snail combinations ditches, the densities of G. truncatula in 2002 and 2006 and control groups. A similar method was also used for were close to each other, whatever the quadrant consid- results noted with A. hypnorum and O. glabra. All the ered and no significant difference between the 2 years was analyses were performed using Statview 5.0 software (SAS noted (Fig. 3(C)). Institute Inc., Cary, NC, USA). In the other experimental ditches, the density of A. hypnorum in 2008 did not show significant variations among quadrants (Fig. 4(A)). The three quadrants located Results at the upstream extremity of these sites showed only the presence of O. glabra in 2008, with snail densities Field investigations significantly lower than in 2002 (Fig. 4(B)). The control popuations of O. glabra occupied the greater part of their A. hypnorum completely colonized road ditches inhab- habitat in 2002 and 2008, and all the differences between ited by G. truncatula in 4 years (2002–2005) (Fig. 2(A)). snail densities recorded during these 2 years were not In the case of G. truncatula, there was a progressive significant (Fig. 4(C)). reduction of ditch lengths from 2002 to 2008 so that the lymnaeid in 2008 only occupied 8.7% of its habitat at the upstream extremity. Like for G. truncatula habitats in which the physid was introduced, complete colonization Laboratory investigations of ditches by A. hypnorum and the progressive limitation of lengths occupied by the lymnaeid were also noted Tables 1 and 2 give the numbers of surviving lymnaeids in habitats occupied by O. glabra (Fig. 2(B)). In 2008, in snail combinations (A. hypnorum+G. truncatula or the O. glabra populations only inhabited 21.6% of their O. glabra) and control groups at the end of the 1-month original sites and were found at the upstream extremity period. In both species of lymnaeids, similar results were of their habitats (Fig. 2(B)). In the control groups, noted. The life stage of A. hypnorum had a significant G. truncatula (Fig. 2(C)) and O. glabra (Fig. 2(D)) occu- influence (G. truncatula: H=30.48, P<0.001; O. glabra: pied the major or total length of their habitats throughout H=28.96, P<0.001) on survival of each lymnaeid. the entire study. The life stage of each lymnaeid and the interaction In ditches inhabited by A. hypnorum and G. truncatula, between the life stages of the physid and the lymnaeid the density of the physid remained somewhat stable had no clear effect on these results. In snail combi- at 14.9–30.6 snails.mx2 in the final year, with statis- nations, the survival of lymnaeids was significantly tically similar densities among quadrants (Fig. 3(A)). lower for adult G. truncatula (P<0.001) and O. glabra G. truncatula was found in 2008 only in two quadrants (P<0.001) than for intermediates (G. truncatula: P<0.01; at the upstream end of its habitat with densities that were O. glabra: P<0.01). In contrast, the survival of juvenile D. Rondelaud et al.: Ann. Limnol. - Int. J. Lim. 52 (2016) 379–386 383

Fig. 3. Distribution of Aplexa hypnorum and Galba truncatula in eight 1-m2 quadrants, located from downstream to upstream, in 2002 and 2008: habitats colonized by A. hypnorum (3A) and G. truncatula (3B), or by G. truncatula only (3C). Graph 3B: significant differences (P<0.01) between 2002 and 2008 (*).

Fig. 4. Distribution of A. hypnorum and Omphiscola glabra in eight 1-m2 quadrants, located from downstream to upstream, in 2002 and 2008: habitats colonized by A. hypnorum (4A) and O. glabra (4B), or by O. glabra only (4C). Graph 4B: significant differences (P<0.01) between 2002 and 2008 (*). lymnaeids was similar to that noted in the corresponding beginning of the experiment). In the control groups, the controls. percentages were 93.4, 97.4 and 98.7%, respectively On day 30 of the experiment, the survival rates (data not shown). of A. hypnorum in snail combinations were 92.0% for No sign of lymnaeid predation by A. hypnorum was juveniles, 97.4% for intermediates, and 100% for adults noted in the different snail combinations formed with (out of a total of 75 individuals in each group at the G. truncatula or O. glabra. In contrast, several cadavers 384 D. Rondelaud et al.: Ann. Limnol. - Int. J. Lim. 52 (2016) 379–386

Table 1. Mean numbers (SD) of Galba truncatula surviving at the end of a 1-month period in pairwise combinations formed by Aplexa hypnorum+G. truncatula (25+50 snails per combination, respectively) and control groups (50 G. truncatula per group). Number (SD) of live G. truncatula Snail group Life stage of A. hypnorum Juveniles Intermediates Adults Snail couples Juveniles 38.3 (7.9) 41.6 (8.3) 45.2 (6.4) Intermediates 24.0 (2.7) 18.7 (5.2) 11.2 (5.2) Adults 5.1 (1.6) 3.0 (0.9) 1.5 (1.4) Controls No physids 45.3 (3.7) 47.9 (2.1) 49.6 (0.5)

Table 2. Mean numbers (SD) of Omphiscola glabra surviving at the end of a 1-month period in pairwise combinations formed by Aplexa hypnorum+O. glabra (25+50 snails per combination, respectively) and control groups (50 O. glabra per group). Number (SD) of live O. glabra Snail group Life stage of A. hypnorum Juveniles Intermediates Adults Snail couples Juveniles 43.2 (7.1) 46.1 (3.9) 47.4 (2.1) Intermediates 37.0 (5.2) 31.8 (7.2) 24.8 (5.4) Adults 9.6 (3.7) 7.5 (2.9) 3.7 (1.5) Controls No physids 45.7 (4.2) 48.2 (1.1) 49.8 (0.3) of juvenile and intermediate lymnaeids after exit from 1999) have already reported the marginalization of most their shells were partly eaten by pre-adult and adult G. truncatula habitats at the peripheral extremity of open A. hypnorum. drainage and rainwater-draining furrows. According to these authors, G. truncatula was outcompeted by other lymnaeids, including O. glabra which may even drive Discussion G. truncatula to local extinction (Rondelaud et al., 2005). Our results demonstrate that A. hypnorum also exerted Among the freshwater gastropods that live in peri- an evident negative effect on O. glabra, though to a lesser odically dried habitats present in Western Europe, extent than on G. truncatula because of the two following A. hypnorum, G. truncatula and O. glabra were considered reasons: (i) the complete colonization of O. glabra habitats to be the most able to withstand drying of their habitats by the physid took longer than that of the other lymnaeid (Kerney, 1999; Anderson, 2006; Glo¨ er and Diercking, (7 years instead of 4 years, respectively: Figs. 2(A) and 2010). Their ability to resist this process is thought to be (B)); and (ii) the populations of O. glabra in their habitats species specific. A. hypnorum was able to resist drought invaded by A. hypnorum occupied greater areas in 2008 at the egg stage (Den Hartog and De Wolf, 1962). In and their sizes were larger than those noted for contrast, the eggs of both lymnaeids did not withstand G. truncatula. summer drying. Juvenile and pre-adult O. glabra bur- On day 30 of the experiment, the survival of each rowed into the soft mud at the beginning of summer lymnaeid in snail combinations significantly decreased drying and aestivated at a depth of 1–6 cm when the when the shell height of A. hypnorum increased (Tables 1 bottom sediment was marl (Rondelaud et al., 2003). In and 2), suggesting that the inhibitory action of the same way, the juvenile and pre-adult G. truncatula A. hypnorum over the lymnaeids seems to be higher when could also burrow into the upper layers of the soil, mainly the physid actively grows in size. This inhibition essentially at altitude (Goumghar et al., 2001) or settle on a support affected adult lymnaeids and, to a lesser extent, inter- structure that varies in nature depending on the type of mediates, whereas the juveniles did not seem to suffer from habitat (Rondelaud et al., 2009). the presence of the physid. As competition of one species In road ditches occupied by G. truncatula or O. glabra, over another had an effect on survivorship, growth or the introduction of A. hypnorum was followed by pro- reproduction of the individuals concerned (Begon et al., gressive colonization of the entire area by the physid and 1996), the low values noted in the intermediate and adult gradual reduction of areas occupied by the lymnaeid lymnaeids are more difficult to comment, as only snail towards the upstream extremity of the habitats. The strong survival was considered in the present study. Because resistance of A. hypnorum eggs to desiccation (Den Hartog A. hypnorum was never observed to prey on live lymnaeids and De Wolf, 1962) and its high mobility (the physid and the three species fed on lettuce and grass leaves that moves more quickly than lymnaeids) may partly explain were given ad libitum, the most reliable hypothesis is to colonization of experimental ditches by this species. In incriminate the mucus of intermediate and adult physids addition, the size of the lymnaeid population significantly that may be toxic for the other freshwater gastropods. decreased over 7 years of the study, so that values noted Several arguments support this last hypothesis. When in 2008 were significantly lower than those recorded in G. truncatula and O. glabra were raised together in the 2002. In contrast, mean densities were relatively stable at same breeding Petri dishes, the former species quickly sites only occupied by G. truncatula or O. glabra. Several died when its shell height reached 6 mm, while the latter authors (Økland, 1990; Moens, 1991; Vareille-Morel et al., survived longer up to the maximum height limit of the D. Rondelaud et al.: Ann. Limnol. - Int. J. Lim. 52 (2016) 379–386 385 adult stage. According to Dreyfuss et al. (2006), this rapid References death of G. truncatula at the adult stage may be due to the toxicity of the mucus secreted by adult O. glabra. Abrous M., Rondelaud D., Dreyfuss G. and Cabaret J., 1999. Another argument comes from the planarian predation Infection of Lymnaea truncatula and Lymnaea glabra by experiment described by Lombardo et al. (2012): planar- Fasciola hepatica and Paramphistomum daubneyi in farms of ians, whose body size was roughly the same as most central France. Vet. Res., 30, 113–118. temperate-climate freshwater snails (y10–15 mm in body Abrous M., Rondelaud D. and Dreyfuss G., 2000. A field study length), often hunted by roaming and leaving a mucus trail of natural infections in three freshwater snails with Fasciola in which small prey such as juvenile P. acuta may become hepatica and/or Paramphistomum daubneyi in central France. entangled. The planarians then revisited the mucus trail J. Helminthol., 74, 189–194. and obtained an “easy meal”. In contrast, larger snails Anderson R., 2006. Aplexa hypnorum – moss bladder snail. such as adults were too large to become entangled in the Northern Ireland Priority Species, Accessed online 11 May planarian mucus. However, one could question whether 2015, http://www.habitas.org.uk/priority/species.asp?item= the mucus hypothesis is applicable in the field, like it is 6624. based on laboratory data. The mucus of A. hypnorum may Bauer B. and Ringeis B., 2002. Changes in gastropod assem- be physically and/or chemically unstable in situ, with soft blages in freshwater habitats in the vicinity of Basel sediment and water flow that could bury it in sediment (Switzerland) over 87 years. Hydrobiologia, 479, 1–10. and/or reduce its toxicity. Begon M., Harper J. and Townsend C., 1996. Ecology: Owing to food that was given ad libitum to snails in Individuals, Populations and Communities (3rd edn), Blackwell Science, Oxford, 1068 p. their aquaria, the results noted in the laboratory experi- ment excluded the occurrence of exploitation competition Brown D.S., 1994. Freshwater Snails of Africa and their Medical Importance, Taylor & Francis Ltd., London, 606 p. and suggested evidence of strong interference competition between the physid and either lymnaeid. Several previous Brown K., 1982. Resource overlap and competition in pond snails: an experimental analysis. Ecology, 63, 412–422. authors had already reported cases of interference compe- tition. Gresens (1995) found that snails (Physa gyrina) had Costil K., Dussart G.B.J. and Daguzan J., 2001. Biodiversity of aquatic gastropods in the Mont St-Michel basin (France) in a strong effect on reproductive output and, consequently, relation to salinity and drying of habitats. Biodiv. Cons., 10, on densities of coexisting chironomid and chydorid crus- 1–18. taceans, even if trophic resources (periphyton) were Den Hartog C., 1963. The distribution of the snail Aplexa not depleted. According to this author, chironomids and hypnorum in Zuid-Beveland in relation to soil and salinity. chydorids were less active in the snail’s presence, showing Basteria, 27, 8–17. an interference effect on behaviour. The reciprocal effect Den Hartog C. and de Wolf L., 1962. The life cycle of the water of chironomids and chydorids on snails was much lower snail Aplexa hypnorum. Basteria, 26, 61–88. so that the snails were declared as the “winners”. Other Dillon R.T. Jr., 2004. The Ecology of Freshwater Molluscs cases of interference competition for freshwater gastro- (2nd edn), Cambridge University Press, Cambridge, 523 p. pods were also reported, for example, by Brown (1982) Dillon R.T. Jr., Watson B.T., Stewart T.W. and Reeves W.K., and Lombardo and Cooke (2004). 2006. The freshwater gastropods of North America. This interspecific competition between A. hypnorum Accessed online 11 May 2015, http://www.fwgna.org. and either lymnaeid requires 7 years in the field to reach Dreyfuss G., Vignoles P., Mekroud A. and Rondelaud D., 2006. complete colonization of the lymnaeid habitat by the The presence of uninfected Omphiscola glabra in a breeding physid, a reduction of areas occupied by the lymnaeid, and of infected Galba truncatula enhanced the characteristics a limitation of its population size. These results suggest of snail infections with Fasciola hepatic. Parasitol. Res., 99, that A. hypnorum was a poor competitor. It is possible 197–199. to question whether these effects in periodically dried Dreyfuss G., Vignoles P. and Rondelaud D., 2010. Omphiscola ditches persist over time. Indeed, even though P. acuta glabra (Gastropoda, Lymnaeidae): changes occurring was considered a competitor in Egypt (El-Hassan, 1974), in natural infections with Fasciola hepatica and populations of this species often co-existed with planor- Paramphistomum daubneyi when this snail species is intro- bids in other countries in Africa (Brown, 1994). duced into new areas. Ann. Limnol. - Int. J. Lim., 46, 191–197. In conclusion, the presence of A. hypnorum in habitats colonized by G. truncatula or O. glabra resulted in a El-Hassan A.A., 1974. Helisoma tenuis and Physa acuta snails as biological means of control against Bulinus truncatus and progressive decrease in areas occupied by lymnaeids and Biomphalaria alexandrina. Proc. Third Int. Congr. Parasitol., their population size. This interspecific competition Mu¨nchen, 3, 1597–1598. Facta Publication, Verlag H. between the physid and either lymnaeid may not be Egeramann, Vienna. due to food present in their habitat, but might be due Glo¨ er P. and Diercking R., 2010. Atlas der Su¨ ßwassermollusken to the toxicity of mucus secreted by intermediate and Hamburg. Rote Liste, Verbreitung, O¨ kologie. adult A. hypnorum. Umweltbeho¨ rde, Hamburg, 182 p. Accessed online 11 May 2015, http://www.malaco.de/Sonderdrucke/atlas-suesswas- sermollusken.pdf. Acknowledgements. The authors would like to thank Glo¨ er P. and Meier-Brook C., 2003. Su¨ sswassermollusken. Ein Dr J. Cook-Moreau for revising the English text. Bestimmungsschlu¨ ssel fu¨ r die Bundesrepublik Deutschland 386 D. Rondelaud et al.: Ann. Limnol. - Int. J. Lim. 52 (2016) 379–386

(13th edn), Deutscher Jugendbund fu¨ r Naturbeobachtung, Rondelaud D., Hourdin P., Vignoles P., Dreyfuss G. and Hamburg, 134 p. Cabaret, J., 2011. The detection of snail host habitats in Goumghar M.D., Rondelaud D., Dreyfuss G. and Benlemlih M., liver fluke infected farms by use of plant indicators. Vet. 2001. Influence of aestivation on the survival of Galba Parasitol., 181, 166–173. truncatula (Mollusca: Gastropoda) populations according Rondelaud D., Djuikwo Teukeng F.F., Vignoles P. and to altitude. Ann. Limnol. - Int. J. Lim., 37, 211–217. Dreyfuss G., 2015. Lymnaea glabra: progressive increase Gresens S.E., 1995. Grazer diversity, competition and the in susceptibility to Fasciola hepatica through successive response of the periphytic community. Oikos, 73, 336–346. generations of experimentally infected Lymnaea glabra. Kerney M., 1999. Atlas of the Land and Freshwater Molluscs J. Helminthol., 89, 398–403. of Britain and Ireland. Harley Books, Colchester, 272 p. Shapiro S.S. and Wilk M.B., 1965. An analysis of variance Lombardo P. and Cooke G.D., 2004. Resource use and test for normality (complete samples). Biometrika, 52, partitioning by two co-occurring freshwater gastropod 591–611. species. Arch. Hydrobiol., 159, 229–251. Siegel S. and Castellan N.J. Jr., 1988. Nonparametric Statistics Lombardo P., Miccoli F.P., Mastracci T., Giustini M. for the Behavioral Sciences (2nd edn), McGraw-Hill, and Cicolani B., 2012. Predation by Dugesia polychroa New York, 399 p. (Platyhelminthes: Tricladida) prevents the establishment of Spyra A., 2010. Environmental factors influencing the occur- Physa acuta (Gastropoda: Pulmonata) in hard-substratum rence of freshwater snails in woodland water bodies. habitats. Folia Malacol., 20, 121–134. Biologia, 65, 697–703. Moens R., 1991. Factors affecting Lymnaea truncatula popula- Taylor E.L., 1965. Fascioliasis and the liver-fluke. FAO tions and related control measures. J. Med. Appl. Malacol., 3, Agricultural Studies, Rome, No. 64, 235 p. 73–84. Torgerson P. and Claxton J., 1999. Epidemiology and control. Mosimann C., 2000. Molluskengesellschaften ausgewa¨ hlter In: Dalton J.P. (ed.), Fasciolosis, CABI Publishing, Oxon, Gewa¨ sser in der Petite Camargue Alsacienne. Doctorate 113–149. Thesis, University of Basel, Basel, Switzerland, 136 p. Vareille-Morel C., Dreyfuss G. and Rondelaud D., 1999. Økland J., 1990. Lakes and Snails. Environment and The characteristics of habitats colonized by three species Gastropods in 1,500 Norwegian Lakes, Ponds and Rivers, of Lymnaea in swampy meadows on acid soil: their interest Universal Book Services/Dr. W. Backhuys, Oegstgeest, for fasciolosis control. Ann. Limnol. - Int. J. Lim., 35, The Netherlands, 516 p. 173–178. Rondelaud D., Vignoles P. and Dreyfuss G., 2003. Field Vignoles P., Rondelaud D. and Dreyfuss G., 2015. La Limne´ e observations on the aestivation of Omphiscola glabra e´ troite (Omphiscola glabra O.F. Mu¨ ller, 1774) : l’abondance (Gastropoda, Lymnaeidae) uninfected or infected with des mollusques adultes dans le centre de la France par Fasciola hepatica in central France. Ann. Limnol. - Int. J. rapport a` la nature ge´ ologique du sol et la pre´ sence d’autres Lim., 39, 129–133. Pulmone´ s aquatiques dans les meˆ mes habitats. MalaCo, 11, Rondelaud D., Hourdin P., Vignoles G. and Dreyfuss G., 2005. 1–5. The contamination of wild watercress with Fasciola hepatica Welter-Schultes F., 2012. European Non-marine Molluscs, in central France depends on the ability of several lymnaeid a Guide for Species Identification. Bestimmungsbuch fu¨ r snails to migrate upstream towards the beds. Parasitol. Res., europa¨ ische Land- und Su¨ sswassermollusken, Planet Poster 95, 305–309. Editions, Go¨ ttingen, 760 p. Rondelaud D., Vignoles P., Dreyfuss G. and Mage C., 2006. Welter-Schultes F., 2013. Species summary for Aplexa hypnorum. The control of Galba truncatula (Gastropoda: Lymnaeidae) AnimalBase, SUB Go¨ ttingen. Accessed online 11 May by the terrestrial snail Zonitoides nitidus on acid soils. 2015, http://www.animalbase.uni-goettingen.de/zooweb/ Biol. Control, 39, 290–299. servlet/AnimalBase/home/species?id =1872. Rondelaud D., Vignoles P. and Dreyfuss G., 2009. La Limne´ e Zbikowska E., 2011. One snail – three Digenea species, tronque´ e, un mollusque d’inte´ reˆ tme´ dical et ve´ te´ rinaire, different strategies in host-parasite interaction. Anim. Biol. PULIM, Limoges, 283 p. 61, 1–19.